Binocular stereopsis is the ability to use differences between the images presented to the two eyes (binocular disparities) to perceive the three dimensional structure of the outside world. The geometry of binocular vision ensures that these differences take a particular form: an image on one part of the right retina can be almost exactly matched to an equivalent image region on the left retina by a horizontal translation. Understanding how neurons are able to signal these disparities is an excellent model system for studying how neuronal processing generates useful perceptual representations. ? ? Current explanations for this mechanism rely upon linear processing of the monocular images. We show that this results in neuronal responses that devote part of their dynamic range to impossible stimuli. In order to determine whether cortical neurons have this unexpected property, we conducted two studies in which sinusoidal luminance gratings were summed. We manipulated the interocular phase difference of each grating component independently. In a stimulus with just two components, we were able to explore all possible combinations. Within this space of combinations, natural disparities (pure translation) all fall along a single line. We found that approximately half of the neurons we studied in the striate cortex did indeed show maximal responses for unnatural combinations of interocular phase. The other half, however, all showed maximal responses to natural stimuli, in a way that current models do not explain. We developed a modification of the binocular energy model that was able to explain the experimental data. One attraction of the new model is that it could also be applied to the outputs of the striate cortex, and hence might explain some of the transformations in binocular signals that occur in extrastriate cortex. ? ? The new model makes a distinctive prediction about responses to stimuli with many sinusoidal components, if the interocular phase differences are manipulated in a particular fashion. We recorded the responses of neurons in the striate cortex, and in the first extrastriate area (V2) to this manipulation. Responses in both areas confirmed the predications of the model. Furthermore, quantitative analysis of the responses from V2 neurons indicated that they did not simply inherit this property from disparity selective neurons in striate cortex. Rather, the mechanism proposed in our model seems to operate in the projection from V1 to V2.

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National Eye Institute (NEI)
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U.S. National Eye Institute
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Bredfeldt, C E; Read, J C A; Cumming, B G (2009) A quantitative explanation of responses to disparity-defined edges in macaque V2. J Neurophysiol 101:701-13
Haefner, Ralf M; Cumming, Bruce G (2008) Adaptation to natural binocular disparities in primate V1 explained by a generalized energy model. Neuron 57:147-58
Read, Jenny C A; Cumming, Bruce G (2007) Sensors for impossible stimuli may solve the stereo correspondence problem. Nat Neurosci 10:1322-8
Nienborg, Hendrikje; Cumming, Bruce G (2007) Psychophysically measured task strategy for disparity discrimination is reflected in V2 neurons. Nat Neurosci 10:1608-14
Bredfeldt, Christine E; Cumming, Bruce G (2006) A simple account of cyclopean edge responses in macaque v2. J Neurosci 26:7581-96
Nienborg, Hendrikje; Cumming, Bruce G (2006) Macaque V2 neurons, but not V1 neurons, show choice-related activity. J Neurosci 26:9567-78
Read, Jenny C A; Cumming, Bruce G (2005) Effect of interocular delay on disparity-selective v1 neurons: relationship to stereoacuity and the pulfrich effect. J Neurophysiol 94:1541-53
Read, Jenny C A; Cumming, Bruce G (2005) The stroboscopic Pulfrich effect is not evidence for the joint encoding of motion and depth. J Vis 5:417-34
Read, Jenny (2005) Early computational processing in binocular vision and depth perception. Prog Biophys Mol Biol 87:77-108
Read, Jenny C A; Cumming, Bruce G (2004) Understanding the cortical specialization for horizontal disparity. Neural Comput 16:1983-2020

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